Oecologia (2005) 142: 474–479 DOI 10.1007/s00442-004-1731-z

GLOBAL CHANGE ECOLOGY

Montserrat Vila` Æ John L. Maron Æ Laia Marco Evidence for the enemy release hypothesis in perforatum

Received: 26 March 2004 / Accepted: 17 September 2004 / Published online: 3 November 2004 Springer-Verlag 2004

Abstract The enemy release hypothesis (ERH), which habitats (Cox 1999). The impact of alien species can has been the theoretical basis for classic biological con- depend largely on both the size of their introduced trol, predicts that the success of invaders in the intro- geographical range and their abundance where intro- duced range is due to their release from co-evolved duced (Parker et al. 1999). Traditionally, there has been natural enemies (i.e. herbivores, pathogens and preda- a general perception that plant invaders are very abun- tors) left behind in the native range. We tested this dant (i.e. large population sizes) and attain larger stature prediction by comparing herbivore pressure on native compared to conspecifics in the native range (Elton European and introduced North American populations 1958). However, empirical evidence supporting these of (St John’s Wort). We found impressions is surprisingly scanty. Only recently have that introduced populations occur at larger densities, are researchers begun to rigorously examine the demogra- less damaged by herbivory and suffer less mor- phy of plant invaders in the introduced and in the native tality than populations in the native range. However, range. These studies have generally found higher seed- overall population size was not significantly different ling establishment and greater overall plant densities in between ranges. Moreover, on average plants were sig- the introduced than native range (Grigulis et al. 2001; nificantly smaller in the introduced range than in the Paynter et al. 2003). There is also some observational native range. Our survey supports the contention that confirmation that certain plant species are larger in their plants from the introduced range experience less herbi- introduced versus native range and that these differences vore damage than plants from the native range. While are genetically based (Crawley 1987; Blossey and No¨ tz- this may lead to denser populations, it does not result in old 1995; Buckley et al. 2003). Nevertheless, when a larger plant size in the introduced versus native range as large number of species have been compared this trend is postulated by the ERH. not always found. For example, a screening of floras has shown that on average European plants invading Cali- Keywords Biological control Æ Herbivory Æ Plant fornia are not significantly taller than in Europe, and invasions Æ Natural enemies hypothesis Æ St John’s Wort Californian plants invading Europe are even smaller than in California (The´baud and Simberloff 2001). To fully establish whether plants from the introduced range perform better than those in the native range, extensive Introduction field surveys must be conducted where introduced and native populations are compared (Willis and Forrester Biological invasions are worldwide phenomena with 2000; Leger and Rice 2003). often devastating effects on native species and natural When differences in plant size exist, the enemy release hypothesis (ERH) has been proposed as an explanation. The ERH posits that one of the leading causes of in- M. Vila` (&) Æ L. Marco creased vigour of some invaders in the introduced range Centre de Recerca Ecolo` gica i Aplicacions Forestals, is liberation from co-evolved natural enemies (i.e. her- Universitat Auto` noma de Barcelona, 08193 Bellaterra, Spain ` E-mail: [email protected] bivores, pathogens and predators) (Maron and Vila Tel.: +34-93-5813584 2001). ERH predicts that plants in the introduced range Fax: +34-93-5814151 are less damaged by natural enemies than in the native J. L. Maron range and this reduction in herbivore pressure translates Division of Biological Sciences, to demographic advantages that result in larger popu- University of Montana, Missoula, MT 59812, USA lation and plant sizes than in the native range. The few 475 studies that have compared levels of herbivory between of live and recently dead H. perforatum plants per unit the native and the introduced range have found that area. If the population was very large (>100 plants), we abundance and diversity of phytophagous randomly sampled 30 plants from within the larger (Memmott et al. 2000) and herbivory and pathogen population. For each plant in the population we re- damage is greater in native than in introduced popula- corded whether individuals showed any evidence of tions (Mitchell et al. 2003; Wolfe 2001). Only one study aboveground herbivore damage. Herbivore damage was has simultaneously compared herbivore pressure, pop- assessed by noting whether plants were defoliated or had ulation density and plant sizes between invaders in their other signs of insect damage such as browsed twigs. native and introduced range (Jakobs et al. 2004). In each population, we randomly selected 20 plants We examined rates of herbivory, plant population (or from ten to 20 if the population had <20 plants) that densities, and plant sizes of the perennial herb Hyperi- were 2 m from each other to ensure they were not con- cum perforatum L. (Guttiferae), in its native range in nected underground. On each plant we measured the Europe and in a portion of its introduced range in number of upright stems, the height of the tallest stem western North America. If the ERH is correct, we would and two perpendicular diameters of the projected plant expect to find introduced populations to be larger, area. denser and less damaged than native populations, and We compared the proportion of populations with North American plants to be larger than European herbivore damage and the presence of dead plants be- plants. tween the two ranges (i.e. native and introduced) with a v2-test. Differences in population size, plant density and the percentage of plants with herbivore damage and Materials and methods percentage plant mortality within a population were compared with a Mann-Whitney test. Differences in Study species plant size (number of stems and plant volume) were compared with a nested ANOVA with region and pop- Hypericum perforatum is a widespread noxious invader ulation within region as random factors. Plant volume 2 native to Europe, North Africa and Asia and introduced (V) was estimated as V=H·p·(D1+D2)/4) where D1 into America, Australasia and South Africa (Weber and D2 are the two perpendicular diameters of the plant 2003). H. perforatum was first introduced into western crown and H is the height of the tallest stem. Because North America in the mid 1800s. By 1943 it had spread plants grow as clumps of many upright stems, cylindrical to >200,000 ha of rangeland in California (Holloway volume is a reasonable measure of overall plant size and and Huffaker 1951). H. perforatum contains secondary is strongly correlated with above-ground plant biomass compounds that are phototoxic and can affect the tissues (Maron et al. 2004). We transformed data to ln or arcsin of grazing insects and mammals (Knox and Dodge if necessary. Means±SE are given. 1985). To control this weed, in the mid 1940s, the defoliating chrysomelid , quadrigemina Fo¨ rster (Coleoptera: Chrysomelidae) was introduced as Results a biocontrol agent (Huffaker and Holloway 1949; Hol- loway and Huffaker 1951). In 1951, biological control We found that 70% of the European populations had had successfully established colonies in all Cali- plants with signs of insect herbivore damage. In con- fornia counties and had markedly reduced H. perfora- trast, in western North America only 28% of the pop- tum populations (Holloway and Huffaker 1951). ulations contained plants that showed evidence of herbivore damage (X2=10.92, P=0.001). The intensity of the damage within each population was also higher in Field survey Europe, where on average 23.39±4.26% of the plants had clear signs of herbivory compared to 3.60±1.46% From mid June to mid July 2003 we simultaneously of the introduced plants (Mann-Whitney, z=3.82, conducted a survey of 25 H. perforatum populations in P=0.0001). In the introduced range, none of the H. the introduced range in California and southern Oregon, perforatum plants were dead, while in Europe 32.5% of and 40 populations within the native range across Eur- the populations had some dead plants (X2=3.28, ope (Table 1). The survey was conducted at the stage of P=0.001). On average, the percentage of dead plants plant flowering. To overcome differences in phenology, within native populations was 5.45±1.98%. we were careful to first survey populations in lower Plant population density (Mann-Whitney, z=4.71, latitudes and altitudes, and with an acute Mediterranean P<0.0001) but not population size (Mann-Whitney, climate. Within each region (Europe and North Amer- z=0.32, P=0.75) was significantly different between ica), we sampled populations that were at least 20 km regions. Populations in western North America had apart and <1,500 m in elevation. We sampled popula- more plants per square metre (1.65±0.56) than in Eur- tions that consisted of groups of more than ten flowering ope (0.17±0.04). Plant volume was also significantly plants interspaced within a 100 m radius within the same different based on the region of plant origin habitat type. In each population we counted the number (F1, 63=34.89, P<0.0001). On average, plants in western 476

Table 1 Information of Range Location Code Latitude () Habitat

Introduced Piercy 101 39.96 Grassland Miranda 102 40.24 Ruderal Hwy 101 103 40.45 Woodland Lake Shasta 104 40.66 Woodland Trinity Lake 105 40.69 Woodland Litte Brown’s 106 40.70 Woodland Big Flat 107 40.74 Grassland Del Lane 108 40.81 Woodland Arcata 109 40.83 Ruderal Titlow 110 40.87 Ruderal Dunsmuir III 111 40.99 Woodland Dunsmuir II 112 41.24 Ruderal Dunsmuir I 113 41.25 Ruderal Gasket 114 41.42 Ruderal Edgewood 115 41.44 Grassland Hwy 3 116 41.62 Ruderal Hwy 199 117 41.84 Grassland Knoppi 118 41.92 Woodland Yreka 119 42.17 Grassland Sarape 120 42.42 Ruderal Rogue River 121 42.43 Ruderal Campjoy 122 42.50 Ruderal Frontage 123 42.70 Ruderal Elk Creek 124 42.85 Woodland Day’s Creek 125 42.96 Ruderal Native Constantina (Spain) 1 37.92 Grassland Fte. Ovejuna (Spain) 2 38.27 Grassland Beneixida (Spain) 3 39.08 Ruderal Picassent (Spain) 4 39.37 Woodland Vall d’Uixo´(Spain) 5 39.83 Orchard Torreblanca (Spain) 6 40.23 Orchard Ulldecona (Spain) 7 40.61 Old field Sant Cugat (Spain) 8 41.47 Grassland Igualada (Spain) 9 41.58 Grassland Callu´s (Spain) 10 41.73 Grassland Ponts (Spain) 11 41.91 Ruderal Solsona (Spain) 12 41.99 Grassland Barbastro (Spain) 13 42.05 Grassland Selva de Mar (Spain) 14 42.33 Grassland Castillo de Jaca (Spain) 15 42.67 Meadow Cuxac (France) 16 43.40 Woodland Les Sangsues (France) 17 43.61 Grassland Lacaune (France) 18 43.68 Woodland Sainte Affrique (France) 19 43.96 Ruderal Millau (France) 20 44.31 Woodland Rodez (France) 21 44.41 Ruderal Figeac (France) 22 44.64 Ruderal Rocamadour (France) 23 44.78 Grassland Uzerche (France) 24 45.43 Ruderal Saint Paul (France) 25 45.73 Grassland Bessines (France) 26 46.12 Woodland Delemont (Switzerland) 27 47.37 Ruderal Bonhomme (France) 28 48.17 Ruderal Baccarat (France) 29 48.44 Ruderal Wettstetten (Germany) 30 48.82 Ruderal Seurenholz (Germany) 31 48.95 Old field Pans (France) 32 49.20 Ruderal St Saens (France) 33 49.64 Ruderal Foucarmont (France) 34 49.80 Woodland Verdun (France) 35 49.80 Ruderal Nouvion (France) 36 50.17 Ruderal Hypericum perforatum Berck (France) 37 50.38 Grassland populations surveyed in the Wasserknoden (Germany) 38 50.70 Woodland introduced range in western Saltzer (Germany) 39 51.49 Ruderal North America and the native Lettewitz (Germany) 40 51.58 Old field range in Europe 477

Fig. 1 Mean plant volume and mean number of stems (+SE) of bar represents the mean of a population ordered according to Table Hypericum perforatum from introduced western North America 1. The two initial left-hand bars of the histograms are the regional (black bars) and native European (white bars) populations. Each means, i.e. the means of the population means for each region

North America were smaller than in Europe (Fig. 1) but sp. and Fusarium oxysporum (Maron et al. in press). plants did not differ in the number of stems per plant Other studies have also found that populations in the (F1, 63=0.03, P<0.86) (Fig. 1). Within regions, there native range are more damaged and host more herbi- were significant differences in H. perforatum volumes vores than in the introduced range (Memmott et al. (F63, 1240=12.14, P<0.0001) and number of stems 2000; Wolfe 2002; Jakobs et al. 2004). (F63, 1240=11.53, P<0.0001) among populations (Fig. 1). H. perforatum form denser populations in western North American than in Europe. However, contrary to theory, plants from the introduced range were not larger Discussion than plants from the native range. In fact, even if they did not differ in the number of stems per plant, plants Our study supports the ERH prediction in that H. per- from the introduced range were smaller than in the na- foratum are less damaged by insect herbivores in the tive range. This suggests that the lower herbivore pres- introduced range than in the native range. Furthermore, sure in the introduced than in the native range did not in the native range 32% of populations contained at translate into higher allocation to plant growth as pre- least one dead plant (and often more), whereas in the dicted by the ERH. These results are in accordance with introduced range mortality was nil. While we cannot be data we have collected from multiple common garden certain, plant mortality in the native range was likely experiments in which we found no evidence that plants caused by pathogen attack or extensive root boring from North American populations are, on average, (Wapshere 1984; Julien and Griffiths 1998). Most dead larger than plants from European populations (Maron plants had the same symptoms that plants infected by et al. 2004). In another experiment we have also found the generalist fungi Colletotrichum sp., Alternaria Nees that North American plants are not better interspecific 478 competitors than are European plants (Vila` et al. 2003). Holloway and Huffaker 1951), although there have been Not only did our survey provide no evidence of in- no recent re-assessments as to how well H. perforatum creased plant size in response to enemy release (as pos- continues to be controlled. Given that H. perforatum has tulated by the ERH), but, in fact, plants in North been under biocontrol in western North America, it is America that supported insect herbivores were larger possible that our results could be influenced by some (0.68±0.12 m3) than herbivore-free plants (0.2±0.01 unknown history of biological control agent attack. In m3). In contrast, in Europe, there were no significant the introduced range, our observations suggest that at differences between plants with (0.58±0.12 m3) and least some H. perforatum populations undergo boom- without (0.62±0.05 m3) defoliation. bust dynamics (J. L. Maron, personal observation). That There are several possibilities for why we found larger is, plants erupt from a seedbank, grow in dense patches, variation in plant volume among European (coefficient and then are found by biocontrol agents which bring of variation=1.29) than North American (coefficient of these incipient populations under control. In the native variation=1.05) plants. One possibility is that North range, we have also witnessed the colonization of dis- American plants were founded by a small subset of turbed areas by large populations which subsequently European individuals and hence there has been a bot- crash due to pathogen attack (M. Vila` , unpublished tleneck that has resulted in decreased variation among data). As far as we know, no one has quantified differ- introduced plants. However, our previous work has ences in dynamics between native and introduced popu- clearly indicated that there have been multiple intro- lations, so it is difficult to know precisely how our results ductions of H. perforatum into North America (Maron might be influenced by biological control in western et al. 2004). Furthermore, based on amplified fragment North America. Nevertheless, given that H. perforatum length polymorphism molecular markers we found as has been a target for biocontrol, our results represent an much neutral genetic variation among introduced plants extremely conservative test of the ERH. In cases where as we did among native plants. In addition to this, in introduced plants have been controlled by biocontrol common gardens introduced plants exhibit as much if agents for several decades, it might be expected that some not more phenotypic variation than native European of the ERH predictions (e.g. larger plant size among plants (Maron et al. 2004). Thus a more likely possibility introduced plants) might fail. for the greater variation in size among European versus Species invasions represent excellent ecological North American plants is that populations were sur- ‘‘experiments’’ that can be used to test hypothesis veyed across a greater latitudinal range in Europe than regarding the evolutionary and ecological mechanisms in North America. of colonization and the nature of interspecific interac- It is probable that plants from the introduced range tions of founder populations. Our survey is the first to are smaller than native European plants due to greater find that despite lower herbivore damage in the intro- intraspecific competition generated by higher plant duced than in the native range, introduced plants are densities in the introduced range. This is supported by a smaller than natives. negative correlation between plant density and mean r plant volume (Spearman rank correlation s=À0.33, Acknowledgements We are tremendously grateful to Libby Van- P=0.009). This explanation was also suggested for the wyhe and Jennifer Williams for helping with the field survey, and invasive Cytisus scoparius. C. scoparius plants grow Daniel Sol and four anonymous reviewers for comments on an more densely where they have been introduced, in earlier draft of the paper. This study was partially funded by NSF Australia and New Zealand, than in native European grant DB00-98377 to J. L. M. and by DGICYT (REN2000-0361/ GLO) to M. V. populations. 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